Plant morphology and behavior of Simmondsia chinensis in the Colorado Desert

Sarah Eskander1, Kayla M. Kettmann2, Jeramy Ott3, Sarah Payne4

1University of California, Riverside; 2University of California, Berkeley; 3University of California, Santa Cruz; 4University of California, Los Angeles

ABSTRACT

At the edges of its range in the Colorado Desert, jojoba (Simmondsia chinensis) has been known to exhibit local morphological adaptations not found elsewhere in its distribution. In this study, we expand upon jojoba’s known sexually dimorphic adaptations and examine its behavioral adaptations to a xeric environment. Specifically, we investigate how jojoba avoids intense solar radiation through leaf orientation. We found that jojoba does not exhibit paraheliotropic leaf tracking but instead orients its leaves to point toward the sun at midday. This behavior is supported by both directional measurements and relative shade cast by jojoba’s leaves throughout the day.

Keywords: Simmondsia chinensis, plant behavior, leaf orientation, sexual dimorphism, paraheliotropism

INTRODUCTION such as tumbleweeds use wind to disperse seeds across the landscape, mesquite has A species’ distribution is often limited by roots that tap into the water table up to 30 environmental extremes that dictate the meters deep, and cacti have modified leaves species’ ability to survive and reproduce. At that protect them from grazers and the sun the fringes of a species’ range, efficient (Rainbow 1974). Tepary beans, grown in the energy allocation is essential for survival southwestern United States, protect (Caughley et al. 1988). Different abiotic themselves from excessive sun exposure factors across a species’ range will cause through paraheliotropism (Yu and Berg variation in available energy, which leads to 1994). This behavior is when plants orient localized physiological adaptations. Such their leaves parallel to the sun to reduce the adaptations may help the species survive amount of solar radiation they receive and reproduce at its range margins (Fisher et (Ehleringer and Forseth 1980). Avoiding sun al. 2009). exposure is an important adaptation that is Desert plants in particular have specific necessary for plants that exist where water adaptations to withstand stressors including is scarce. high temperatures, wind, solar radiation, As a dioecious evergreen shrub that has and low precipitation (Oerth 1983). Species adapted to the low precipitation and high

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temperatures of the desert, jojoba tracks on the southern half of the sky in the (Simmondsia chinensis) is an ideal study Northern Hemisphere. Understanding species that can be used to understand how jojoba’s morphological and behavioral plants adapt at their range margins. Its range adaptations will further our knowledge of extends from the Mojave Desert to Baja how species respond to environmental California (Wallace 1979). At the northern stressors on the edge of their ranges. edge of its range in California, jojoba exhibits adaptations like sexually dimorphic shrub METHODS size and leaf size. Compared to males, females have larger and thicker leaves that 2.1 Natural History of the Study Site retain more water to be used to form their Located at 33.1005° N, 116.3013° W, Anza- larger reproductive structures. Females have Borrego Desert State Park occupies the to allocate 30–40 percent of their resources eastern side of the granitic Peninsular to reproductive structures while males only Ranges in San Diego County. From June to use 10–15 percent. To further examine September, Anza-Borrego’s monthly sexual dimorphism in jojoba, we extreme temperatures routinely surpass investigated trichome and stomata density. 43°C until they dip below 38°C in November. We predicted to find more trichomes and The park occasionally sees extreme low fewer stomata on female jojobas because temperatures down to -7°C. Anza-Borrego trichomes have been shown to reduce averages 15.75 cm of rain per year. The visible light absorption and therefore reduce majority of the park contains open desert evapotranspiration through a leaf’s stomata scrub, which is home to jojoba along with (Rewald et al. 2012). creosote bush, ocotillo, teddybear cholla, Preliminary observations suggest that and California barrel cactus. changes in morphology are not the only Our four study sites (Figure 1) are all ways jojoba has adapted to stressful located near Borrego Springs, California, conditions—behavior may play a role. toward the northern end of the park. The Although “behavior” is not often used when elevation at Borrego Springs is 245 meters discussing plants, it has been described as an above sea level. The temperature during our organism’s ability to react to its environment five days of the study, Nov. 2 to Nov. 6, 2018, in order to increase fitness (Van Loon 2015). remained around 30°C and the weather We predict that jojoba will increase its remained clear. The last rainfall in Borrego fitness in a xeric environment by orienting its Springs, 0.69 cm, occurred on Nov. 13 and leaf tips to point toward the sun. 14, 20 days prior to the start of our study. Paraheliotropism would be beneficial because it minimizes leaf surface exposure to the sun, thereby reducing desiccation (Berg 1990). Alternatively, jojoba leaves might not solar track but instead position themselves with leaf tips pointing south. A south-facing orientation might reduce harsh solar radiation at midday because the sun

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2.2.2 Camera Traps

To test if jojoba is heliotropic we set out two camera traps. One camera trap was placed facing a female jojoba and the other toward a male jojoba. The camera traps took a picture every 15 minutes for 24 hours. We then viewed the pictures and noted if the angle of the leaves or branches changed.

2.2.3 Staked Branches and Leaves

In order to further test if jojobas exhibit paraheliotropic behavior, we created two manipulations to assess branch and leaf movement. We selected three male and three female jojobas and chose two Figure 1. Research locations. The four sites (red branches on the southern side of each bush. pins) are located in Anza-Borrego Desert State Park For branch “A” we focused on position of the near Borrego Springs, San Diego County, California. branch itself and for branch “B” we focused on the position of five axial leaves. Using a 2.2 Research design compass and clinometer, we recorded 2.2.1 Male versus Female Leaf Morphology direction and angle from the ground, which we hereafter call “dip.” On branch A, we To test for differences between male and staked the branch at approximately 10 cm female leaves’ stomata density, we from its base so it was parallel to the ground identified five male and five female plants at but its axial end was free to move. We then Site 1 (Figure 1). We collected two leaves used two stakes to hold down branch B. One near the tip of a south-facing branch 1 m stake was placed near the base of the branch from the ground on each jojoba. We then and the other about 10 cm from the tip so it performed a leaf peel using clear nail polish was parallel to the ground but the leaves and viewed the peel slide under a were free to move. After manipulation, we microscope. We counted the hairs and re-measured the direction and dip of branch stomata on the adaxial and abaxial surfaces A and the five leaves on branch B. After five of each leaf in a 1 sq. mm. section to days we re-measured the direction and dip determine if there is a difference between of branch A and the leaves on branch B. the sexes. To test if there was a difference between male and female leaf size, we 2.2.4 Cardinal Directions measured the leaf length, width, and To determine if jojoba leaves orient thickness from 18 different jojobas (nine themselves to point south, we measured the males and nine females) at all four sites. direction that the leaf tips were pointing using a compass. We also recorded dip using

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a clinometer. Jojoba leaves are decussate, squares containing shade, estimating to the meaning each leaf pair is cross-stacked to nearest half-square. form an alternating pattern. To account for both orientations, we took the 2.3 Statistical Analysis measurement of the top two pairs of leaves at each cardinal direction. We chose leaves Statistical analyses were conducted using that were at the top of the plant in order to JMP statistical software v.14 and Python minimize the effect of the leaves being with Jupyter Notebook. We used JMP to run shaded by their own canopy. At each site, we a t-test for differences in leaf thickness, leaf noted the angle of the horizon in the east area, leaf direction (sine and cosine), and the and west to determine the time of sunrise, dip of the leaf between the sexes. We used sunset, and midday. an ANOVA to see how cardinal direction affects dip and direction (sine and cosine). 2.2.5 Shade Platform We used a paired t-test to compare branch direction, branch dip, leaf direction, and leaf We performed a shade experiment at two dip before and after manipulation. We used of our four sites. We began by selecting eight a regression to test for a quadratic male and seven female jojobas. On each of relationship with the shade platform data to the plants we chose an axial cluster of leaves find the relative shade minimum. We also on a south-facing branch. To measure the used Python to create circular histograms relative sun exposure of jojoba leaves at with cardinal direction data and to calculate different times of day, we constructed a 20 average direction of the leaves. by 20 cm cardboard platform with a 1 square cm grid pattern. We cut a 1 cm wide slit from RESULTS the edge of the platform to the center and tied a 10 cm string from the center of the 3.1 Female versus Male Leaf Morphology platform. At the edge of the platform, we There was no difference in the number of affixed a rod that protruded orthogonally stomata (Figure 2), size, direction, or dip of out of the grid. At each jojoba plant, we the leaves between male and female placed the grid 10 cm away from the tip of jojobas. There was a marginal significance in the selected leaf cluster using the string as a number of hairs (N=20, t=1.84, p=0.074) measurement device. To position the (Figure 3). When comparing leaf thickness, platform orthogonally to the sun’s rays, we the male leaves were thicker than female angled the platform so the rod didn’t cast a leaves (N=144, F=5.67 p=0.019) (Figure 4). shadow. With the platform positioned at the 3.2 Camera Traps correct angle and distance, the shadow of the leaves fell on the grid. We repeated the The camera traps did not indicate any process in two-hour intervals from sunrise heliotropic movement in jojoba. (6:10 a.m.) to sunset (4:05 p.m.) for each jojoba. We took a picture of every resulting shadow pattern and counted the number of

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Figure 2. No effect of sex on stomata density. Figure 4. Male jojoba leaves are thicker than female Stomata density was quantified using a peel from leaves. Vertical lines represent ± 1 standard error the abaxial and adaxial surface of each leaf. Stomata from the mean. were counted in 1 sq. mm. sections. Vertical lines represent ±1 standard error from the mean. 3.3 Staked Branches and Leaves

Staked branch A did not change in direction or dip after five days (cosine of direction: N=6, t=1.22, p=0.28) (sine of direction: N=6, t=1.12, p=0.31) (Dip: N=6, t=0.06, p=0.96). For branch B the direction and dip of the leaves did not noticeably change after five days (cosine of direction: N=30, t=1.57, p=0.13) (sine of direction: N=30, t=0.03, p=0.98) (Dip: N=30, t=1.88, p=0.07).

3.4 Cardinal Direction

Figure 3. Female leaves have higher trichome density than male leaves. Stomata density was The average direction of all leaves was quantified using a peel from the abaxial and adaxial 155°, pointing southeast. This corresponded surface of each leaf. Trichomes were counted in 1 to the direction of the sun at approximately sq. mm. sections. Vertical lines represent ± 1 10:10 a.m. North-facing leaves had the most standard error from the mean. variation in direction, east-facing leaves tended to point southeast, south-facing leaves pointed south and southeast, and west-facing leaves pointed southwest (cosine of direction: N=138, F=5.22, p=0.0019) (sine of direction: N=138, F=32.2,

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p<0.0001). North-facing leaves were more vertical than the others (N=144, F=2.80, p=0.0422) (Figure 5).

3.5 Shade Platform

The leaves were oriented to create the least shade at 10:41 a.m. (N=15, Quadratic r²=0.377, Quadratic p<0.001, Linear r²=0.051, Linear p=0.059) (Figure 6). Earlier and later in the day, they receive more direct sunlight on their leaf surfaces. Figure 6. Jojoba leaves cast smallest shadow at midday. Quadratic regression of the relative amount of shade cast by the jojoba leaves during different times of day. Each point represents one shade measurement.

DISCUSSION

4.1 Female Versus Male Leaf Morphology

Our results comparing the difference between male and female leaves differ from previously conducted research. Prior studies in Anza-Borrego and Joshua Tree found that female leaves are thicker compared to males, which is the opposite of our results Figure 5. Jojoba leaves point southeast. Center. A (Wallace 1979; Kohorn 1995). Our results circular scatter plot represents direction of jojoba leaves from all sides of the plant. Each dot may deviate from previous studies due to represents one leaf. The red dot represents the the small number of sites we sampled and average leaf direction. Left, right, top, bottom. Each their close proximity to each other. These circular histogram represents leaves from a findings suggest that landscape-level particular side of the plant. The bars show the variation may be a determinant for number of leaves pointing a certain direction. 0° represents north, 90° represents east, 180° thickness. represents south, and 270° represents west. 4.2 Camera Traps

Our study did not indicate any heliotropic movement in jojobas. Plants enact heliotropic movement by adjusting their turgor pressure throughout the day. Constant adjustment of pressure requires

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manipulation of water in the base of the leaf for Anza-Borrego is shifted approximately 30 (Moore and Hines 2017). Historically, jojobas minutes earlier to 11:15 a.m.—only one might not have existed in locations with hour earlier than our average leaf direction enough water availability to adopt of 155.34°. This direction corresponds to the heliotropic behaviors. It may be more energy sun’s position at 10:10 a.m. The difference in efficient to instead be oriented parallel to direction of the sun between 11:15 a.m. and the sun’s rays during midday. 10:10 a.m. is only 18°. This slight discrepancy could be due to imprecise measurements or 4.3 Staked Branches and Leaves potentially confounding variables such as When manipulated, the leaves and site. On the north side of the bush, leaves branches did not re-adjust to be more have the most variable orientation. We parallel to the sun’s rays. We believe that believe this is due to leaves on the north side five days might be too short of a time period of the bush receiving more shade from the to detect a change in direction or dip. If the rest of the plant compared to other staked branches were left for a few months, directions, so they wouldn’t need to protect the branches or leaves might have moved to themselves from direct sunlight. have less sun exposure. This behavior has These results for dip are contradictory to been documented in other plants based on the Comstock and Mahall (1985) study, seasons. Leaf movements in Ceanothus are which found that two Ceanothus shrubs had motivated by varying water availability at more vertical inclinations on south-facing different times of the year (Comstock and leaves, an adaptation to increase solar Mahall 1985). The leaves in our study moved absorption when water availability is high. over the course of months, not days. Jojoba exhibits the opposite pattern due to low water availability. By minimizing direct 4.4 Cardinal Directions and Shade Platform sunlight, the jojoba leaves are preventing water loss and desiccation. Desert plants often arrange their leaves permanently perpendicular to the sun’s rays 4.5 Significance and Future Studies to reduce harmful irradiance and heat accumulation (Ehleringer and Forseth 1980). To survive the intense solar radiation and Our results suggest that jojobas follow this arid conditions of its range margin, jojoba pattern. On the east, south, and west side of has both morphological and behavioral the bush, leaves were oriented south to adaptations. Our results for leaf morphology southeast. We believe they point south were different than those found by previous because in the northern hemisphere the sun studies, indicating that the local tracks in the southern part of the sky. This environment may influence how the plants behavior allows the plants to reduce their express sexual dimorphic traits. Cardinal exposure to solar radiation. We believe they direction and shade platform tests both point east because the mountain range to indicate that jojoba has a behavioral the west extends up to 9° above the true response to the sun’s location in the sky. In horizon, making the sun set about one hour future studies, jojoba may be transplanted earlier than true sunset. As a result, midday to other locations to see if its morphological

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and behavioral adaptations are genetic or Fischer, B., B. Taborsky, and U. Dieckmann. 2009. habitat-dependent. Understanding if jojoba Unexpected patterns of plastic energy allocation in stochastic environments. The American Naturalist. is genetically predisposed or can adjust to a 173(3):E108-E120. xeric habitat may help us understand how plants with similar morphology or behavior Kohorn, L. 1995. Geographic variation in the might fare in a drying environment. occurrence and extent of sexual dimorphism in a Increasing desertification is causing dioecious shrub, Simmondsia chinensis. Oikos 74(1):137–145. organisms to either adapt or disappear (Rogers 1977). It is important for us to Loon, A. F. V. 2015. Hydrological drought explained. continue to research physiological WIREs Water 2:359–392. adaptations, whether morphological or behavioral, because they are essential for Moore, J. and A. Hines. 2017. Biomimetic engineering analysis of heliotropic plants. Transdisciplinary species’ survival. Journal of Engineering & Science 8:36–53.

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